[en] Chronic cold exposure is detrimental to chill susceptible insects that may accumulate chill injuries. To cope with deleterious effects of cold temperature, insects employ a variety of physiological strategies and metabolic adjustments, such as production of cryoprotectants, or remodeling of cellular membranes. Cold tolerance is a key element determining the fundamental niche of species. Because Drosophila suzukii is an invasive fruit pest, originating from East Asia, knowledge about its thermal biology is urgently needed. Physiological mechanisms underlying cold tolerance plasticity remain poorly understood in this species. Here, we explored metabolic and lipidomic modifications associated with the acquisition of cold tolerance in D. suzukii using Omics technologies (LC- and GC-MS/MS). In both cold-acclimated males and females, we observed physiological changes consistent with homeoviscous/homeophasic adaptation of membranes: reshuffling of phospholipid head groups and increasing unsaturation rate of fatty acids. Modification of fatty acids unsaturation were also observed in triacylglycerides, which would likely increase accessibility of lipid reserves. At the metabolic level, we observed clear-cut differentiation of metabolic profiles with cold-acclimated metabotypes showing accumulation of several potential cryoprotectants (sugars and amino acids). Metabolic pathway analyses indicated a remodeling of various processes, including purine metabolism and aminoacyl tRNA biosynthesis. These data provide a large-scale characterization of lipid rearrangements and metabolic pathway modifications in D. suzukii in response to cold acclimation and contribute to characterizing the strategies used by this species to modulate cold tolerance.
Disciplines :
Entomology & pest control Anatomy (cytology, histology, embryology...) & physiology Environmental sciences & ecology
Author, co-author :
Enriquez, Thomas ; Université de Liège - ULiège > Département GxABT > Gestion durable des bio-agresseurs ; Université Rennes 1, Centre National de la Recherche Scientifique , Rennes , France
Colinet, Hervé; Université Rennes 1, Centre National de la Recherche Scientifique , Rennes , France
Language :
English
Title :
Cold acclimation triggers lipidomic and metabolic adjustments in the spotted wing drosophila Drosophila suzukii (Matsumara).
Publication date :
01 June 2019
Journal title :
American Journal of Physiology - Regulatory Integrative and Comparative Physiology
ANR - Agence Nationale de la Recherche [FR] FWF - Austrian Science Fund [AT]
Funding text :
This work has been funded by the SUZUKILL project (The French National Research Agency: ANR-15-CE21-0017 and the Austrian Science Fund, FWF:I 2604-B25).
Bahrndorff S, Petersen SO, Loeschcke V, Overgaard J, Holmstrup M. Differences in cold and drought tolerance of high arctic and sub-arctic populations of Megaphorura arctica Tullberg 1876 (Onychiuridae: Col-lembola). Cryobiology 55: 315–323, 2007. doi:10.1016/j.cryobiol.2007. 09.001.
Bashan M, Akbas H, Yurdakoc K. Phospholipid and triacylglycerol fatty acid composition of major life stages of sunn pest, Eurygaster integriceps (Heteroptera: Scutelleridae). Comp Biochem Physiol B Biochem Mol Biol 132: 375–380, 2002. doi:10.1016/S1096-4959 (02)00045-3.
Bashan M, Cakmak O. Changes in composition of phospholipid and triacylglycerol fatty acids prepared from prediapausing and diapausing individuals of Dolycoris baccarum and Piezodorus lituratus (Heterop-tera: Pentatomidae). Ann Entomol Soc Am 98: 575–579, 2005.
Bennett VA, Pruitt NL, Lee RE Jr. Seasonal changes in fatty acid composition associated with cold-hardening in third instar larvae of Eurosta solidaginis. J Comp Physiol B 167: 249 –255, 1997. doi:10.1007/s003600050071.
Cacela C, Hincha DK. Low amounts of sucrose are sufficient to depress the phase transition temperature of dry phosphatidylcholine, but not for lyoprotection of liposomes. Biophys J 90: 2831–2842, 2006. doi:10. 1529/biophysj.105.074427.
Calabria G, Máca J, Bächli G, Serra L, Pascual M. First records of the potential pest species Drosophila suzukii (Diptera: Drosophilidae) in Europe. J Appl Entomol 136: 139 –147, 2012. doi:10.1111/j.1439-0418. 2010.01583.x.
Cao-Hoang L, Dumont F, Marechal PA, Gervais P. Inactivation of Escherichia coli and Lactobacillus plantarum in relation to membrane permeabilization due to rapid chilling followed by cold storage. Arch Microbiol 192: 299 –305, 2010. doi:10.1007/s00203-010-0555-y.
Carpenter JF, Crowe JH. The mechanism of cryoprotection of proteins by solutes. Cryobiology 25: 244 –255, 1988. doi:10.1016/0011-2240(88)90032-6.
Carvalho M, Sampaio JL, Palm W, Brankatschk M, Eaton S, Shevchenko A. Effects of diet and development on the Drosophila lipidome. Mol Syst Biol 8: 600, 2012. doi:10.1038/msb.2012.29.
Chong J, Soufan O, Li C, Caraus I, Li S, Bourque G, Wishart DS, Xia J. MetaboAnalyst 4.0: towards more transparent and integrative metabolomics analysis. Nucleic Acids Res 46: W486 –W494, 2018. doi:10.1093/nar/gky310.
Colinet H, Larvor V, Laparie M, Renault D. Exploring the plastic response to cold acclimation through metabolomics: Metabolomics of cold acclimation response. Funct Ecol 26: 711–722, 2012. doi:10.1111/j.1365-2435.2012.01985.x.
Colinet H, Nguyen TTA, Cloutier C, Michaud D, Hance T. Proteomic profiling of a parasitic wasp exposed to constant and fluctuating cold exposure. Insect Biochem Mol Biol 37: 1177–1188, 2007. doi:10.1016/j.ibmb.2007.07.004.
Colinet H, Renault D. Metabolic effects of CO2 anaesthesia in Drosophila melanogaster. Biol Lett 8: 1050 –1054, 2012. doi:10.1098/rsbl. 2012.0601.
Colinet H, Renault D. Similar post-stress metabolic trajectories in young and old flies. Exp Gerontol 102: 43–50, 2018. doi:10.1016/j.exger. 2017.08.021.
Colinet H, Renault D, Javal M, Berková P, Šimek P, Koštál V. Uncovering the benefits of fluctuating thermal regimes on cold tolerance of drosophila flies by combined metabolomic and lipidomic approach. Biochim Biophys Acta 1861: 1736–1745, 2016. doi:10.1016/j.bbalip. 2016.08.008.
Cooper BS, Hammad LA, Fisher NP, Karty JA, Montooth KL. In a variable thermal environment selection favors greater plasticity of cell membranes in Drosophila melanogaster. Evolution 66: 1976 –1984, 2012. doi:10.1111/j.1558-5646.2011.01566.x.
Cooper BS, Hammad LA, Montooth KL. Thermal adaptation of cellular membranes in natural populations of Drosophila melanogaster. Funct Ecol 28: 886–894, 2014. doi:10.1111/1365-2435.12264.
Cossins AR. Temperature Adaptation of Biological Membranes. Portland, OR: Portland Press, 1994.
Cossins AR, Murray PA, Gracey AY, Logue J, Polley S, Caddick M, Brooks S, Postle T, Maclean N. The role of desaturases in cold-induced lipid restructuring. Portland Press Limited, 2002.
Crowe JH, Crowe LM, Carpenter JF, Rudolph AS, Wistrom CA, Spargo BJ, Anchordoguy TJ. Interactions of sugars with membranes. Biochim Biophys Acta 947: 367–384, 1988. doi:10.1016/0304-4157(88)90015-9.
Dalton DT, Walton VM, Shearer PW, Walsh DB, Caprile J, Isaacs R. Laboratory survival of Drosophila suzukii under simulated winter conditions of the Pacific Northwest and seasonal field trapping in five primary regions of small and stone fruit production in the United States. Pest Manag Sci 67: 1368 –1374, 2011. doi:10.1002/ps.2280.
David RJ, Gibert P, Pla E, Petavy G, Karan D, Moreteau B. Cold stress tolerance in Drosophila: analysis of chill coma recovery in D. melanogaster. J Therm Biol 23: 291–299, 1998. doi:10.1016/S0306-4565(98)00020-5.
Denlinger DL, Lee RE Jr (Eds.). Low Temperature Biology of Insects. New York: Cambridge University Press, 2010.
Ditrich T, Koštál V. Comparative analysis of overwintering physiology in nine species of semi-aquatic bugs (Heteroptera: Gerromorpha). Physiol Entomol 36: 261–270, 2011. doi:10.1111/j.1365-3032.2011. 00794.x.
Dray S, Dufour A-B. The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22: 1–20, 2007. doi:10.18637/jss. v022.i04.
Enriquez T, Colinet H. Basal tolerance to heat and cold exposure of the spotted wing drosophila, Drosophila suzukii. PeerJ 5: e3112, 2017. doi:10.7717/peerj.3112.
Enriquez T, Renault D, Charrier M, Colinet H. Cold acclimation favors metabolic stability in Drosophila suzukii. Front Physiol 9: 1506, 2018. doi:10.3389/fphys.2018.01506.
Everman ER, Freda PJ, Brown M, Schieferecke AJ, Ragland GJ, Morgan TJ. Ovary development and cold tolerance of the invasive pest Drosophila suzukii (Matsumura) in the central plains of Kansas, United States. Environ Entomol 47: 1013–1023, 2018. doi:10.1093/ee/nvy074.
Foray V, Desouhant E, Voituron Y, Larvor V, Renault D, Colinet H, Gibert P. Does cold tolerance plasticity correlate with the thermal environment and metabolic profiles of a parasitoid wasp? Comp Biochem Physiol A Mol Integr Physiol 164: 77–83, 2013. doi:10.1016/j.cbpa.2012. 10.018.
Fox J, Weisberg S. An R Companion to Applied Regression (2nd ed.). Thousand Oaks, CA: Sage, 2011.
Giavalisco P, Köhl K, Hummel J, Seiwert B, Willmitzer L. 13C isotope-labeled metabolomes allowing for improved compound annotation and relative quantification in liquid chromatography-mass spectrom-etry-based metabolomic research. Anal Chem 81: 6546–6551, 2009. doi:10.1021/ac900979e.
Goodhue RE, Bolda M, Farnsworth D, Williams JC, Zalom FG. Spotted wing drosophila infestation of California strawberries and raspberries: economic analysis of potential revenue losses and control costs. Pest Manag Sci 67: 1396 –1402, 2011. doi:10.1002/ps.2259.
Goto SG, Katagiri C. Effects of acclimation temperature on membrane phospholipids in the flesh fly Sarcophaga similis. Entomol Sci 14: 224 –229, 2011. doi:10.1111/j.1479-8298.2010.00439.x.
Goto SG, Udaka H, Ueda C, Katagiri C. Fatty acids of membrane phospholipids in Drosophila melanogaster lines showing rapid and slow recovery from chill coma. Biochem Biophys Res Commun 391: 1251– 1254, 2010. doi:10.1016/j.bbrc.2009.12.053.
Guan XL, Cestra G, Shui G, Kuhrs A, Schittenhelm RB, Hafen E, van der Goot FG, Robinett CC, Gatti M, Gonzalez-Gaitan M, Wenk MR. Biochemical membrane lipidomics during Drosophila development. Dev Cell 24: 98 –111, 2013. doi:10.1016/j.devcel.2012.11.012.
Hahn DA, Denlinger DL. Energetics of insect diapause. Annu Rev Entomol 56: 103–121, 2011. doi:10.1146/annurev-ento-112408-085436.
Hamby KA, Bellamy DE, Chiu JC, Lee JC, Walton VM, Wiman NG, York RM, Biondi A. Biotic and abiotic factors impacting development, behavior, phenology, and reproductive biology of Drosophila suzukii. J Pest Sci 89: 605–619, 2016. doi:10.1007/s10340-016-0756-5.
Hammad LA, Cooper BS, Fisher NP, Montooth KL, Karty JA. Profiling and quantification of Drosophila melanogaster lipids using liquid chromatography/mass spectrometry. Rapid Commun Mass Spectrom 25: 2959–2968, 2011. doi:10.1002/rcm.5187.
Hauser M. A historic account of the invasion of Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) in the continental United States, with remarks on their identification. Pest Manag Sci 67: 1352–1357, 2011. doi:10.1002/ps.2265.
Hazel JR. Cold Adaptation in Ectotherms: Regulation of Membrane Function and Cellular Metabolism. In: Animal Adaptation to Cold, edited by Wang LCH. Berlin, Heidelberg: Springer Berlin Heidelberg, 1989, p. 1–50.
Hazel JR. Thermal adaptation in biological membranes: is homeoviscous adaptation the explanation? Annu Rev Physiol 57: 19 –42, 1995. doi:10.1146/annurev.ph.57.030195.000315.
Hazel JR, Williams EE. The role of alterations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment. Prog Lipid Res 29: 167–227, 1990. doi:10.1016/0163-7827(90)90002-3.
Hoffman JM, Soltow QA, Li S, Sidik A, Jones DP, Promislow DEL. Effects of age, sex, and genotype on high-sensitivity metabolomic profiles in the fruit fly, Drosophila melanogaster. Aging Cell 13: 596 –604, 2014. doi:10.1111/acel.12215.
Hosler JS, Burns JE, Esch HE. Flight muscle resting potential and species-specific differences in chill-coma. J Insect Physiol 46: 621–627, 2000. doi:10.1016/S0022-1910(99)00148-1.
Jakobs R, Gariepy TD, Sinclair BJ. Adult plasticity of cold tolerance in a continental-temperate population of Drosophila suzukii. J Insect Physiol 79: 1–9, 2015. doi:10.1016/j.jinsphys.2015.05.003.
Jones HE, Harwood JL, Bowen ID, Griffiths G. Lipid composition of subcellular membranes from larvae and prepupae of Drosophila melanogaster. Lipids 27: 984–987, 1992. doi:10.1007/BF02535576.
Kamatani N, Jinnah HA, Hennekam RC, van Kuilenburg ABP. Purine and pyrimidine metabolism. In: Emery and Rimoin’s Principles and Practice of Medical Genetics, edited by Rimoin D, Pyeritz R, Korf B. New York: Elsevier, 2014, p. 1–38.
Kandror O, DeLeon A, Goldberg AL. Trehalose synthesis is induced upon exposure of Escherichia coli to cold and is essential for viability at low temperatures. Proc Natl Acad Sci USA 99: 9727–9732, 2002. doi:10.1073/pnas.142314099.
Kayukawa T, Chen B, Hoshizaki S, Ishikawa Y. Upregulation of a desaturase is associated with the enhancement of cold hardiness in the onion maggot, Delia antiqua. Insect Biochem Mol Biol 37: 1160 –1167, 2007. doi:10.1016/j.ibmb.2007.07.007.
Kenis M, Tonina L, Eschen R, van der Sluis B, Sancassani M, Mori N, Haye T, Helsen H. Non-crop plants used as hosts by Drosophila suzukii in Europe. J Pest Sci (2004) 89: 735–748, 2016. doi:10.1007/s10340-016-0755-6.
Kimura MT. Cold and heat tolerance of drosophilid flies with reference to their latitudinal distributions. Oecologia 140: 442–449, 2004. doi:10. 1007/s00442-004-1605-4.
Knapp M, Vernon P, Renault D. Studies on chill coma recovery in the ladybird, Harmonia axyridis: Ontogenetic profile, effect of repeated cold exposures, and capacity to predict winter survival. J Therm Biol 74: 275–280, 2018. doi:10.1016/j.jtherbio.2018.04.013.
Koštál V. Cell structural modifications in insects at low temperature. In: Low Temperature Biology of Insects, edited by Denlinger DL and Lee RE Jr. New York: Cambridge University Press, 2010, p. 116 –140.
Kostál V, Berková P, Šimek P. Remodelling of membrane phospholipids during transition to diapause and cold-acclimation in the larvae of Chymomyza costata (Drosophilidae). Comp Biochem Physiol B Biochem Mol Biol 135: 407–419, 2003. doi:10.1016/S1096-4959(03)00117-9.
Koštál V, Korbelová J, Poupardin R, Moos M, Šimek P. Arginine and proline applied as food additives stimulate high freeze tolerance in larvae of Drosophila melanogaster. J Exp Biol 219: 2358 –2367, 2016. doi:10.1242/jeb.142158.
Koštál V, Korbelová J, Rozsypal J, Zahradníčková H, Cimlová J, Tomčala A, Šimek P. Long-term cold acclimation extends survival time at 0°C and modifies the metabolomic profiles of the larvae of the fruit fly Drosophila melanogaster. PLoS One 6: e25025, 2011. doi:10.1371/journal.pone.0025025.
Koštál V, Simek P. Changes in fatty acid composition of phospholipids and triacylglycerols after cold-acclimation of an aestivating insect prepupa. J Comp Physiol B 168: 453–460, 1998. doi:10.1007/s003600050165.
Koštál V, Šimek P, Zahradníčková H, Cimlová J, Štětina T. Conversion of the chill susceptible fruit fly larva (Drosophila melanogaster) to a freeze tolerant organism. Proc Natl Acad Sci USA 109: 3270 –3274, 2012. doi:10.1073/pnas.1119986109.
Koštál V, Vambera J, Bastl J. On the nature of pre-freeze mortality in insects: water balance, ion homeostasis and energy charge in the adults of Pyrrhocoris apterus. J Exp Biol 207: 1509 –1521, 2004. doi:10.1242/jeb. 00923.
Koštál V, Yanagimoto M, Bastl J. Chilling-injury and disturbance of ion homeostasis in the coxal muscle of the tropical cockroach (Nau-phoeta cinerea). Comp Biochem Physiol B Biochem Mol Biol 143: 171–179, 2006. doi:10.1016/j.cbpb.2005.11.005.
Koštál V, Zahradnícková H, Šimek P. Hyperprolinemic larvae of the drosophilid fly, Chymomyza costata, survive cryopreservation in liquid nitrogen. Proc Natl Acad Sci USA 108: 13,041–13,046, 2011. doi:10. 1073/pnas.1107060108.
Lavagnino NJ, Díaz BM, Cichón LI, De La Vega G, Garrido SA, Lago JD, Fanara JJ. New records of the invasive pest Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) in the South American continent. Rev Soc Entomol Argent 77: 27–31, 2018. doi:10.25085/rsea. 770105.
Lee RE Jr. A primer on insect cold-tolerance. In: Low Temperature Biology of Insects edited by Denlinger DL and Lee RE Jr. New York: Cambridge University Press, 2010, p. 3–34.
Lee RE Jr, Damodaran K, Yi S-X, Lorigan GA. Rapid cold-hardening increases membrane fluidity and cold tolerance of insect cells. Cryobiology 52: 459 –463, 2006. doi:10.1016/j.cryobiol.2006.03.003.
Li Y, Zhang L, Chen H, Koštál V, Simek P, Moos M, Denlinger DL. Shifts in metabolomic profiles of the parasitoid Nasonia vitripennis associated with elevated cold tolerance induced by the parasitoid’s diapause, host diapause and host diet augmented with proline. Insect Biochem Mol Biol 63: 34 –46, 2015. doi:10.1016/j.ibmb.2015.05.012.
Lu Y-X, Zhang Q, Xu W-H. Global metabolomic analyses of the hemolymph and brain during the initiation, maintenance, and termination of pupal diapause in the cotton bollworm, Helicoverpa armigera. PLoS One 9: e99948, 2014. doi:10.1371/journal.pone.0099948.
Luévano-Martínez LA, Kowaltowski AJ. Phosphatidylglycerol-de-rived phospholipids have a universal, domain-crossing role in stress responses. Arch Biochem Biophys 585: 90 –97, 2015. doi:10.1016/j.abb. 2015.09.015.
Maclean HJ, Kristensen TN, Sørensen JG, Overgaard J. Laboratory maintenance does not alter ecological and physiological patterns among species: a Drosophila case study. J Evol Biol 31: 530 –542, 2018. doi:10.1111/jeb.13241.
MacMillan HA, Andersen JL, Davies SA, Overgaard J. The capacity to maintain ion and water homeostasis underlies interspecific variation in Drosophila cold tolerance. Sci Rep 5: 18,607, 2015. doi:10.1038/srep18607.
MacMillan HA, Guglielmo CG, Sinclair BJ. Membrane remodeling and glucose in Drosophila melanogaster: a test of rapid cold-hardening and chilling tolerance hypotheses. J Insect Physiol 55: 243–249, 2009. doi:10.1016/j.jinsphys.2008.11.015.
MacMillan HA, Knee JM, Dennis AB, Udaka H, Marshall KE, Merritt TJS, Sinclair BJ. Cold acclimation wholly reorganizes the Drosophila melanogaster transcriptome and metabolome. Sci Rep 6: 28999, 2016. doi:10.1038/srep28999.
MacMillan HA, Williams CM, Staples JF, Sinclair BJ. Reestablish-ment of ion homeostasis during chill-coma recovery in the cricket Gryllus pennsylvanicus. Proc Natl Acad Sci USA 109: 20750 –20755, 2012. doi:10.1073/pnas.1212788109.
Michaud MR, Denlinger DL. Oleic acid is elevated in cell membranes during rapid cold-hardening and pupal diapause in the flesh fly, Sarcophaga crassipalpis. J Insect Physiol 52: 1073–1082, 2006. doi:10. 1016/j.jinsphys.2006.07.005.
Michaud MR, Denlinger DL. Shifts in the carbohydrate, polyol, and amino acid pools during rapid cold-hardening and diapause-associated cold-hardening in flesh flies (Sarcophaga crassipalpis): a metabolomic comparison. J Comp Physiol B 177: 753–763, 2007. doi:10.1007/s00360-007-0172-5.
Ohtsu T, Katagiri C, Kimura MT. Biochemical aspects of climatic adaptations in Drosophila curviceps, D. immigrans, and D. albomicans (Diptera: Drosophilidae). Environ Entomol 28: 968 –972, 1999. doi:10. 1093/ee/28.6.968.
Ohtsu T, Katagiri C, Kimura MT, Hori SH. Cold adaptations in Drosophila. Qualitative changes of triacylglycerols with relation to overwintering. J Biol Chem 268: 1830 –1834, 1993.
Ohtsu T, Kimura MT, Katagiri C. How Drosophila species acquire cold tolerance: qualitative changes of phospholipids. Eur J Biochem 252: 608 –611, 1998. doi:10.1046/j.1432-1327.1998.2520608.x.
Overgaard J, MacMillan HA. The integrative physiology of insect chill tolerance. Annu Rev Physiol 79: 187–208, 2017. doi:10.1146/annurev-physiol-022516-034142.
Overgaard J, Malmendal A, Sørensen JG, Bundy JG, Loeschcke V, Nielsen NC, Holmstrup M. Metabolomic profiling of rapid cold hardening and cold shock in Drosophila melanogaster. J Insect Physiol 53: 1218 –1232, 2007. doi:10.1016/j.jinsphys.2007.06.012.
Overgaard J, Sørensen JG, Petersen SO, Loeschcke V, Holmstrup M. Changes in membrane lipid composition following rapid cold hardening in Drosophila melanogaster. J Insect Physiol 51: 1173–1182, 2005. doi:10.1016/j.jinsphys.2005.06.007.
Overgaard J, Sørensen JG, Petersen SO, Loeschcke V, Holmstrup M. Reorganization of membrane lipids during fast and slow cold hardening in Drosophila melanogaster. Physiol Entomol 31: 328 –335, 2006. doi:10.1111/j.1365-3032.2006.00522.x.
Overgaard J, Tomčala A, Sørensen JG, Holmstrup M, Krogh PH, Šimek P, Kostál V. Effects of acclimation temperature on thermal tolerance and membrane phospholipid composition in the fruit fly Drosophila melanogaster. J Insect Physiol 54: 619 –629, 2008. doi:10.1016/j.jinsphys.2007.12.011.
Panel ADC, Zeeman L, van der Sluis BJ, van Elk P, Pannebakker BA, Wertheim B, Helsen HHM. Overwintered Drosophila suzukii are the main source for infestations of the first fruit crops of the season. Insects 9: 1–18, 2018. doi:10.3390/insects9040145.
Pruitt NL, Lu C. Seasonal changes in phospholipid class and class-specific fatty acid composition associated with the onset of freeze tolerance in third-instar larvae of Eurosta solidaginis. Physiol Biochem Zool 81: 226 –234, 2008. doi:10.1086/524394.
Pujol-Lereis LM, Fagali NS, Rabossi A, Catalá Á, Quesada-Allué LA. Chill-coma recovery time, age and sex determine lipid profiles in Ceratitis capitata tissues. J Insect Physiol 87: 53–62, 2016. doi:10.1016/j.jinsphys.2016.02.002.
Rozsypal J, Koštál V, Berková P, Zahradníčková H, Šimek P. Seasonal changes in the composition of storage and membrane lipids in overwintering larvae of the codling moth, Cydia pomonella. J Therm Biol 45: 124 –133, 2014. doi:10.1016/j.jtherbio.2014.08.011.
Ryan GD, Emiljanowicz L, Wilkinson F, Kornya M, Newman JA. Thermal tolerances of the spotted-wing Drosophila Drosophila suzukii (Diptera: Drosophilidae). J Econ Entomol 109: 746 –752, 2016. doi:10. 1093/jee/tow006.
Santoiemma G, Trivellato F, Caloi V, Mori N, Marini L. Habitat preference of Drosophila suzukii across heterogeneous landscapes. J Pest Sci 92: 485–494, 2019. doi:10.1007/s10340-018-1052-3
Shearer PW, West JD, Walton VM, Brown PH, Svetec N, Chiu JC. Seasonal cues induce phenotypic plasticity of Drosophila suzukii to enhance winter survival. BMC Ecol 16: 1–18, 2016. doi:10.1186/s12898-016-0070-3.
Sinclair BJ, Marshall KE. The many roles of fats in overwintering insects. J Exp Biol 221, Suppl 1: jeb161836, 2018. doi:10.1242/jeb. 161836.
Sinensky M. Homeoviscous adaptation--a homeostatic process that regulates the viscosity of membrane lipids in Escherichia coli. Proc Natl Acad Sci USA 71: 522–525, 1974. doi:10.1073/pnas.71.2.522.
Storey KB, Storey JM. Biochemistry of cryoprotectants. In: Insects at Low Temperature. Boston: Springer, 1991, p. 64 –93.
Dolédec S, Chessel D. Recent developments in linear ordination methods in environmental sciences. Adv Ecol 1: 133–155, 1991.
Teets NM, Peyton JT, Ragland GJ, Colinet H, Renault D, Hahn DA, Denlinger DL. Combined transcriptomic and metabolomic approach uncovers molecular mechanisms of cold tolerance in a temperate flesh fly. Physiol Genomics 44: 764 –777, 2012. doi:10.1152/physiolgenomics. 00042.2012.
Thieringer HA, Jones PG, Inouye M. Cold shock and adaptation. BioEssays 20: 49 –57, 1998. doi:10.1002/(SICI)1521-1878(199801) 20:1<49:AID-BIES8<3.0.CO;2-N.
Thistlewood HMA, Gill P, Beers EH, Shearer PW, Walsh DB, Rozema BM, Acheampong S, Castagnoli S, Yee WL, Smytheman P, Whitener AB. Spatial analysis of seasonal dynamics and overwintering of Drosophila suzukii (Diptera: Drosophilidae) in the Okanagan-Colum-bia basin, 2010-2014. Environ Entomol 47: 221–232, 2018. doi:10.1093/ee/nvx178.
Tomcala A, Tollarová M, Overgaard J, Simek P, Kostál V. Seasonal acquisition of chill tolerance and restructuring of membrane glycerophos-pholipids in an overwintering insect: triggering by low temperature, desiccation and diapause progression. J Exp Biol 209: 4102–4114, 2006. doi:10.1242/jeb.02484.
van Dooremalen C, Ellers J. A moderate change in temperature induces changes in fatty acid composition of storage and membrane lipids in a soil arthropod. J Insect Physiol 56: 178 –184, 2010. doi:10.1016/j. jinsphys.2009.10.002.
Vesala L, Salminen TS, Koštál V, Zahradníčková H, Hoikkala A. Myo-inositol as a main metabolite in overwintering flies: seasonal metabolomic profiles and cold stress tolerance in a northern drosophilid fly. J Exp Biol 215: 2891–2897, 2012. doi:10.1242/jeb.069948.
Wallingford AK, Lee JC, Loeb GM. The influence of temperature and photoperiod on the reproductive diapause and cold tolerance of spotted-wing drosophila, Drosophila suzukii. Entomol Exp Appl 159: 327–337, 2016. doi:10.1111/eea.12443.
Wallingford AK, Loeb GM. Developmental acclimation of Drosophila suzukii (Diptera: Drosophilidae) and its effect on diapause and winter stress tolerance. Environ Entomol 45: 1081–1089, 2016. doi:10.1093/ee/nvw088.
Williams CM, Watanabe M, Guarracino MR, Ferraro MB, Edison AS, Morgan TJ, Boroujerdi AFB, Hahn DA. Cold adaptation shapes the robustness of metabolic networks in Drosophila melanogaster. Evolution 68: 3505–3523, 2014. doi:10.1111/evo.12541.
Yancey PH. Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J Exp Biol 208: 2819 –2830, 2005. doi:10.1242/jeb.01730.
Yocum GD, Žd’árek J, Joplin KH, Lee RE Jr, Smith DC, Manter KD, Denlinger DL. Alteration of the eclosion rhythm and eclosion behavior in the flesh fly, Sarcophaga crassipalpis, by low and high temperature stress. J Insect Physiol 40: 13–21, 1994. doi:10.1016/0022-1910(94)90107-4.
Zachariassen KE. Physiology of cold tolerance in insects. Physiol Rev 65: 799 –832, 1985. doi:10.1152/physrev.1985.65.4.799.
Zeng J-P, Ge F, Su J-W, Wang Y. The effect of temperature on the diapause and cold hardiness of Dendrolimus tabulaeformis (Lepidoptera: Lasiocampidae). Eur J Entomol 105: 599 –606, 2008. doi:10.14411/eje. 2008.080.
Zerulla FN, Schmidt S, Streitberger M, Zebitz CP, Zelger R. On the overwintering ability of Drosophila suzukii in South Tyrol. J Berry Res 5: 41–48, 2015. doi:10.3233/JBR-150089.
